Identification of AnnexinA1 as an Endogenous Regulator of RhoA, and Its Role in the Pathophysiology and Experimental Therapy of Type-2 Diabetes

Front Immunol. 2019 Mar 27:10:571. doi: 10.3389/fimmu.2019.00571. eCollection 2019.

Abstract

Annexin A1 (ANXA1) is an endogenously produced anti-inflammatory protein, which plays an important role in the pathophysiology of diseases associated with chronic inflammation. We demonstrate that patients with type-2 diabetes have increased plasma levels of ANXA1 when compared to normoglycemic subjects. Plasma ANXA1 positively correlated with fatty liver index and elevated plasma cholesterol in patients with type-2 diabetes, suggesting a link between aberrant lipid handling, and ANXA1. Using a murine model of high fat diet (HFD)-induced insulin resistance, we then investigated (a) the role of endogenous ANXA1 in the pathophysiology of HFD-induced insulin resistance using ANXA1-/- mice, and (b) the potential use of hrANXA1 as a new therapeutic approach for experimental diabetes and its microvascular complications. We demonstrate that: (1) ANXA1-/- mice fed a HFD have a more severe diabetic phenotype (e.g., more severe dyslipidemia, insulin resistance, hepatosteatosis, and proteinuria) compared to WT mice fed a HFD; (2) treatment of WT-mice fed a HFD with hrANXA1 attenuated the development of insulin resistance, hepatosteatosis and proteinuria. We demonstrate here for the first time that ANXA1-/- mice have constitutively activated RhoA. Interestingly, diabetic mice, which have reduced tissue expression of ANXA1, also have activated RhoA. Treatment of HFD-mice with hrANXA1 restored tissue levels of ANXA1 and inhibited RhoA activity, which, in turn, resulted in restoration of the activities of Akt, GSK-3β and endothelial nitric oxide synthase (eNOS) secondary to re-sensitization of IRS-1 signaling. We further demonstrate in human hepatocytes that ANXA1 protects against excessive mitochondrial proton leak by activating FPR2 under hyperglycaemic conditions. In summary, our data suggest that (a) ANXA1 is a key regulator of RhoA activity, which restores IRS-1 signal transduction and (b) recombinant human ANXA1 may represent a novel candidate for the treatment of T2D and/or its complications.

Keywords: Annexin A1; Rho A; hepatosteatosis; metabolism; nephropathy; type-2 diabetes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Annexin A1 / blood
  • Annexin A1 / genetics*
  • Annexin A1 / metabolism*
  • Cholesterol / blood
  • Diabetes Mellitus, Experimental / physiopathology*
  • Diabetes Mellitus, Experimental / therapy
  • Diabetes Mellitus, Type 2 / physiopathology*
  • Diabetes Mellitus, Type 2 / therapy
  • Diet, High-Fat / adverse effects
  • Dyslipidemias / physiopathology
  • Fatty Liver / blood
  • Fatty Liver / pathology
  • Humans
  • Hyperglycemia / physiopathology
  • Insulin Receptor Substrate Proteins / metabolism
  • Insulin Resistance / physiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Obesity / physiopathology
  • Receptors, Formyl Peptide / metabolism
  • Receptors, Lipoxin / metabolism
  • rhoA GTP-Binding Protein / metabolism*

Substances

  • ANXA1 protein, human
  • Annexin A1
  • FPR2 protein, human
  • Insulin Receptor Substrate Proteins
  • Irs1 protein, mouse
  • Receptors, Formyl Peptide
  • Receptors, Lipoxin
  • annexin A1, mouse
  • Cholesterol
  • RhoA protein, mouse
  • rhoA GTP-Binding Protein